Mol Hum Reprod 2014 Ramm SA 1

NEW RESEARCH HORIZON Review Sperm competition and the evolution of spermatogenesis Steven A. Ramm 1, * , Lukas Scha ¨ rer 2 , Jens Ehmcke 3 , and Joachim Wistuba 4 1 Evolutionary Biology, Bielefeld University, Morgenbreede 45, 33615 Bielefeld, Germany 2 Evolutionary Biology, Zoological Institute, University of Basel, Vesalgasse 1, 4051 Basel, Switzerland 3 Central Animal Facility of the Faculty of Medicine, University of Mu ¨ nster, Albert-Schweitzer-Campus 1 (A8), 48149 Mu ¨ nster, Germany 4 Institute of Reproductive and Regenerative Biology, Centre of Reproductive Medicine and Andrology, University of Mu ¨ nster, Albert-Schweitzer-Campus 1 (D11), 48149 Mu ¨ nster, Germany *Correspondence address. E-mail: [email protected] Submitted on May 28, 2014; resubmitted on July 7, 2014; accepted on August 15, 2014 abstract: Spermatog enesi s isa longand comp lexprocessthat,despitethe share d over all goalof prod ucingthe malegamete,display s stri king amounts of interspecific diversity. In this review, we argue that sperm competition has been an important selection pressure acting on multiple asp ect s of spermatogenesis, cau sin g var iationin thenumbe r and morph ology of spe rm pr odu ced , and in themolec ula r and cel lul ar proces sesby which this happens. We begin by reviewing the basic biology of spermatogenesis in some of the main animal model systems to illustrate this di- ver sity,and thenask to whatextentthis varia tionarises fromthe evol ution aryforcesacting on spermatoge nesis, mostnotablyspermcompetit ion. Weexplorefive speci fic aspects of spermatogenesi s froman evol ution aryperspect ive,namely:(i) inter speci ficdiversit y in thenumberand morph - ologyof spermproduc ed; (ii)the testi cula r organ izat ions and stemcell syst ems usedto produ ce them; (iii)the largenumberand highevolutio nary rate of genes underpinning spermatogenesis; (iv) the repression of transcription during spermiogenesis and its link to the potential for haploid sel ect ion ; and(v) thepheno men on of sel ect ionactin g at theleve l of thegermline. Ov era ll weconcl udethatadopti ng an evo lutionar y per spe cti ve canshedlighton man y oth erw iseopaqu e fea tures of spe rma togen esis, andhelpto exp lainthediversi tyof wa ysin whichmale s of dif fer entspec ies perform this fundamentally important process. Key words: evolution / spermatogenesis / spermatogonial stem cells / sperm competition / testicular function Introduction Atsomelevel , allspermaimto dothe same thi ng:fert ili zean eggandcon- tribu te the pater nal halfof the resu ltingzygote’ s genome. Whythen does sperm morphology differ so much across the Animal Kingdom, with the male gamete often being considered the most diverse animal cell type known (Pitnick et al., 2009a)? Similarly, each egg only requires one spermto fer til ize it, so whythen do mal es pro duc e sperm in suc h pro di- giousquantiti es, gene rallyfar outn umbe ringthe numberof ovaproduced by females? The answers lie in understanding the evolutionary force of spermcompet ition andthe pro fou nd eff ectit exe rtson mal e rep roduct- ivebiology.In fact,we will arg ue in thi s rev iewthatthink ingaboutsperm- atogenesis in such an evolutionary framework holds great potential for explaining these and many other aspects of this most fundamental of male reproductive traits. But first, what exactly is sperm competition? And why might it be so impor tant ? Put simpl y, sper m comp etition occurs when ever sperm from two or more males compe te to fert ilize a femal e’s eggs (Parker, 1970, 1998). Until quite recently, it was assumed that multiple mating by femal es—and henc e sper m comp etiti on—w as rela tivel y rare in nature, but the advent of DNA fingerprinting technology and other advances have drastically altered that view (see Zeh and Zeh, 2003). Amon g evolu tiona ry biolo gists , spermcompetit ion is now wide ly reco g- nized as a pervasive influence on male reproduction (Birkhead and Møller, 1998; Birkhead et al., 2009). How thenmight spermcompeti tion affec t spermatog enesis? To begin with one major aspect of diversity between species—the numbers of sperm produ ced by the testis—l et us comp are two close ly relat ed species that differ in levels o f sperm competition. Chimpanzees ( Pan tro- glodytes) live in large mult i-ma le, mult i-female grou ps, and femal es typic - ally mate with multiple males. By contrast, the gorilla (Gorilla gorilla) mating system is characterized by a single breeding male who monopo- lizes access to multiple females, thereby ensuring that his sperm do not hav e to comp ete with thos e from poten tial rivals . How would we predict these two mating systems to play out in terms of the investment males should make in sperm production? Presumably in the former case the sperm from one chimpanzee male faces competition from sperm fro m othe r males ov er which of the m fer tili zes the egg . Since the outcome of sperm competition likely often resembles a lottery in which buying more tickets than your compet itors increase s the chances of wi nn ing , this le adsto an arms race ov er sperm numb ersand an ov er allin- crease in male investment towards sperm production. Just as predicted, & The Author 2014. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. For Permissions, please email: [email protected] Mol ecular Human Reproductio n, Vol.0 , No. 0 pp. 1– 11, 2014 doi:10.1093/molehr/gau070 Mol. Hum. Reprod. Advance Access published October 16, 2014 a t U n i v e r s i d a d N a c i o n a l d e C ? r d o b a o O c t o b e r 2 4 , 2 0 1 4 h t t p : / / o l e h r . o x f o r d j o u r a l s . o r g / D o w n l o a d e d f r o m

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Mol Hum Reprod 2014 Ramm SA 1